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Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE (Open Access)

Pre-dispersal seed-predation affects fruit crop and seed fitness in a highly fragmented savanna tree

S. D. Heyes https://orcid.org/0000-0001-5008-2137 A B * , J. W. Morgan A B , S. J. Sinclair https://orcid.org/0000-0002-4282-1021 C , Z. C. Walker D and S. E. Hoebee https://orcid.org/0000-0001-8007-1324 A B
+ Author Affiliations
- Author Affiliations

A Department of Environment and Genetics, La Trobe University, Bundoora, Vic. 3086, Australia.

B Research Centre for Future Landscapes, La Trobe University, Bundoora, Vic. 3086, Australia.

C Arthur Rylah Institute for Environmental Research, Department of Environment, Land, Water and Planning, Heidelberg, Vic. 3084, Australia.

D School of BioSciences, University of Melbourne, Parkville, Vic. 3010, Australia.

* Correspondence to: s.heyes@latrobe.edu.au

Handling Editor: Andrew Denham

Australian Journal of Botany - https://doi.org/10.1071/BT23011
Submitted: 2 February 2023  Accepted: 2 August 2023   Published online: 28 August 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Context: Silver banksia (Banksia marginata) savannas of south-eastern Australia were formerly widespread but are now largely cleared and fragmented, with small populations often showing recruitment limitation. Which may, in part, be due to seed predation by yellow-tailed black cockatoos (Zanda funerea), which have been observed foraging for seed.

Aims: The study aimed to investigate the impact of pre-dispersal seed predation by yellow-tailed black cockatoos on fruit crop between early development and seed release. Additionally, we wanted to assess seed fitness from partially damaged and discarded cones.

Methods: The study quantified silver banksia infructescence removal at four populations between early December and seed release in March. We also quantified seed mass and germinability of seeds from cones removed in December, February and March.

Key results: All populations experienced significant seed predation (>50%), with almost complete removal of cones from some populations. Early removal limits seed release from cones (only 18% of early removed follicles released seed). Further, early removal also significantly reduced seed mass and germination.

Conclusions: Pre-dispersal seed predation by cockatoos is likely to act as a strong filter for recruitment limitation in silver banksia, by negatively affecting annual seed crop size, seed fitness and germinability.

Implications: Our study showed the potential impact fragmentation can have on antagonistic plant–animal interactions. Small, isolated B. marginata populations are likely to continue to decline without active strategies to remedy seed predation such as large-scale restoration.

Keywords: Banksia marginata, fragmentation, germination, granivory, parrots, recruitment limitation, seed, seed predation, Zanda funerea.


References

Ballarin CS, Hachuy-Filho L, Doria MJW, Giffu MM, Polizello DS, Oliveira PH, Lacerda-Barbosa PA, Amorim FW (2022a) Intra-seasonal and daily variations in nectar availability affect bee assemblage in a monodominant afforested Brazilian Cerrado. Austral Ecology 47, 1315–1328.
Intra-seasonal and daily variations in nectar availability affect bee assemblage in a monodominant afforested Brazilian Cerrado.Crossref | GoogleScholarGoogle Scholar |

Ballarin CS, Hachuy-Filho L, Fontúrbel FE, Amorim FW (2022b) Density-dependent effects on the reproductive outcome of a native tree at tropical restored habitats. Forest Ecology and Management 520, 120391
Density-dependent effects on the reproductive outcome of a native tree at tropical restored habitats.Crossref | GoogleScholarGoogle Scholar |

Brannon CH (1927) Life history of the plum curculio (Conotrachelus nenuphar Herbst.). Journal of the Elisha Mitchell Scientific Society 43, 79–83. https://www.jstor.org/stable/24332758

Broadhurst LM, Young AG, Forrester R (2008) Genetic and demographic responses of fragmented Acacia dealbata (Mimosaceae) populations in southeastern Australia. Biological Conservation 141, 2843–2856.
Genetic and demographic responses of fragmented Acacia dealbata (Mimosaceae) populations in southeastern Australia.Crossref | GoogleScholarGoogle Scholar |

Brown PR, Huth NI, Banks PB, Singleton GR (2007) Relationship between abundance of rodents and damage to agricultural crops. Agriculture, Ecosystems & Environment 120, 405–415.
Relationship between abundance of rodents and damage to agricultural crops.Crossref | GoogleScholarGoogle Scholar |

Bureau of Meteorology (2018) Monthly climate statistics. Available at http://www.bom.gov.au

Chacoff NP, Morales JM, Vaquera MdP (2004) Efectos de la Fragmentatión Sobre la Aborción y Depredación de Semillas en el Chaco Serrano. Biotropica 36, 109–117.
Efectos de la Fragmentatión Sobre la Aborción y Depredación de Semillas en el Chaco Serrano.Crossref | GoogleScholarGoogle Scholar |

Chen Q, Tomlinson KW, Cao L, Wang B PMID: (2017) Effects of fragmentation on the seed predation and dispersal by rodents differ among species with different seed size. Integrative Zoology 12, 468–476.
Effects of fragmentation on the seed predation and dispersal by rodents differ among species with different seed size.Crossref | GoogleScholarGoogle Scholar |

Coates-Estrada R, Estrada A, Meritt D (1993) Foraging by parrots (Amazona autumnalis) on fruits of Stemmadenia donnell-smithii (Apocynaceae) in the tropical rain forest of Los Tuxtlas, Mexico. Journal of Tropical Ecology 9, 121–124.
Foraging by parrots (Amazona autumnalis) on fruits of Stemmadenia donnell-smithii (Apocynaceae) in the tropical rain forest of Los Tuxtlas, Mexico.Crossref | GoogleScholarGoogle Scholar |

Coffey K, Benkman CW, Milligan BG (1999) The adaptive significance of spines on pine cones. Ecology 80, 1221–1229.
The adaptive significance of spines on pine cones.Crossref | GoogleScholarGoogle Scholar |

Collins K (2009) ‘Banksias.’ (Bloomings Books: Melbourne, Vic., Australia)

Cowling RM, Lamont BB (1987) Post-fire recruitment of four co-occurring Banksia species. Journal of Applied Ecology 24, 645–658.
Post-fire recruitment of four co-occurring Banksia species.Crossref | GoogleScholarGoogle Scholar |

Dauber J, Biesmeijer JC, Gabriel D, Kunin WE, Lamborn E, Meyer B, Nielsen A, Potts SG, Roberts SPM, Sõber V, Settele J, Steffan-Dewenter I, Stout JC, Teder T, Tscheulin T, Vivarelli D, Petanidou T (2010) Effects of patch size and density on flower visitation and seed set of wild plants: a pan-European approach. Journal of Ecology 98, 188–196.
Effects of patch size and density on flower visitation and seed set of wild plants: a pan-European approach.Crossref | GoogleScholarGoogle Scholar |

Eriksson O, Ehrlén J PMID: (1992) Seed and microsite limitation of recruitment in plant populations. Oecologia 91, 360–364.
Seed and microsite limitation of recruitment in plant populations.Crossref | GoogleScholarGoogle Scholar |

Fleury M, Galetti M (2006) Forest fragment size and microhabitat effects on palm seed predation. Biological Conservation 131, 1–13.
Forest fragment size and microhabitat effects on palm seed predation.Crossref | GoogleScholarGoogle Scholar |

Forsyth SA PMID: (2003) Density-dependent seed set in the Haleakala silversword: evidence for an Allee effect. Oecologia 136, 551–557.
Density-dependent seed set in the Haleakala silversword: evidence for an Allee effect.Crossref | GoogleScholarGoogle Scholar |

Foster BL, Tilman D (2003) Seed limitation and the regulation of community structure in oak savanna grassland. Journal of Ecology 91, 999–1007.
Seed limitation and the regulation of community structure in oak savanna grassland.Crossref | GoogleScholarGoogle Scholar |

Francisco MR, de Oliveira Lunardi V, Galetti M (2002) Massive seed predation of Pseudobombax grandiflorum (Bombacaceae) by parakeets Brotogeris versicolurus (Psittacidae) in a forest fragment in Brazil. Biotropica 34, 613–615.
Massive seed predation of Pseudobombax grandiflorum (Bombacaceae) by parakeets Brotogeris versicolurus (Psittacidae) in a forest fragment in Brazil.Crossref | GoogleScholarGoogle Scholar |

Francisco MR, Lunardi VO, Guimarães PR, Galetti M (2008) Factors affecting seed predation of Eriotheca gracilipes (Bombacaceae) by parakeets in a cerrado fragment. Acta Oecologica 33, 240–245.
Factors affecting seed predation of Eriotheca gracilipes (Bombacaceae) by parakeets in a cerrado fragment.Crossref | GoogleScholarGoogle Scholar |

García D, Chacoff NP PMID: (2007) Scale-dependent effects of habitat fragmentation on hawthorn pollination, frugivory, and seed predation. Conservation Biology 21, 400–411.
Scale-dependent effects of habitat fragmentation on hawthorn pollination, frugivory, and seed predation.Crossref | GoogleScholarGoogle Scholar |

Groom PK, Lamont BB, Duff HC (1994) Self-crypsis in Hakea trifurcata as an avian granivore deterrent. Functional Ecology 8, 110–117.
Self-crypsis in Hakea trifurcata as an avian granivore deterrent.Crossref | GoogleScholarGoogle Scholar |

Grubb PJ (1977) The maintenance of species-richness in plant communities: the importance of the regeneration niche. Biological Reviews 52, 107–145.
The maintenance of species-richness in plant communities: the importance of the regeneration niche.Crossref | GoogleScholarGoogle Scholar |

He T, Lamont BB, Downes KS (2011) Banksia born to burn. New Phytologist 191, 184–196.
Banksia born to burn.Crossref | GoogleScholarGoogle Scholar |

Herrerías-Diego Y, Quesada M, Stoner KE, Lobo JA, Hernández-Flores Y, Sanchez Montoya G (2008) Effect of forest fragmentation on fruit and seed predation of the tropical dry forest tree Ceiba aesculifolia. Biological Conservation 141, 241–248.
Effect of forest fragmentation on fruit and seed predation of the tropical dry forest tree Ceiba aesculifolia.Crossref | GoogleScholarGoogle Scholar |

Heyes SD, Sinclair SJ, Hoebee SE, Morgan JW (2020) How widespread are recruitment bottlenecks in fragmented populations of the savanna tree Banksia marginata (Proteaceae)? Plant Ecology 221, 545–557.
How widespread are recruitment bottlenecks in fragmented populations of the savanna tree Banksia marginata (Proteaceae)?Crossref | GoogleScholarGoogle Scholar |

Hurd AM (1921) Seed-coat injury and viability of seeds of wheat and barley as factors in susceptibility to molds and fungicides. Journal of Agricultural Research 21, 99–122.

Janzen DH (1971) Seed predation by animals. Annual Review of Ecology and Systematics 2, 465–492.
Seed predation by animals.Crossref | GoogleScholarGoogle Scholar |

Jones FA, Comita LS (2010) Density-dependent pre-dispersal seed predation and fruit set in a tropical tree. Oikos 119, 1841–1847.
Density-dependent pre-dispersal seed predation and fruit set in a tropical tree.Crossref | GoogleScholarGoogle Scholar |

Jury G (2023) Pollination vectors of tree-form silver banksia (Banksia marginata, Proteaceae). MSc Thesis, La Trobe University, Melbourne, Vic., Australia.

Krushelnycky PD PMID: (2014) Evaluating the interacting influences of pollination, seed predation, invasive species and isolation on reproductive success in a threatened alpine plant. PLoS ONE 9, e88948
Evaluating the interacting influences of pollination, seed predation, invasive species and isolation on reproductive success in a threatened alpine plant.Crossref | GoogleScholarGoogle Scholar |

Kurkjian HM, Carothers SK, Jules ES (2017) Seed predation has the potential to drive a rare plant to extinction. Journal of Applied Ecology 54, 862–871.
Seed predation has the potential to drive a rare plant to extinction.Crossref | GoogleScholarGoogle Scholar |

Lee J, Finn H, Calver M (2013) Feeding activity of threatened black cockatoos in mine-site rehabilitation in the jarrah forest of south-western Australia. Australian Journal of Zoology 61, 119–131.
Feeding activity of threatened black cockatoos in mine-site rehabilitation in the jarrah forest of south-western Australia.Crossref | GoogleScholarGoogle Scholar |

Long JL (1984) The diets of three species of parrots in the South of Western Australia. Wildlife Research 11, 357–371.
The diets of three species of parrots in the South of Western Australia.Crossref | GoogleScholarGoogle Scholar |

Lunt ID (1997) Tree densities last century on the lowland Gippsland plain, Victoria. Australian Geographical Studies 35, 342–348.
Tree densities last century on the lowland Gippsland plain, Victoria.Crossref | GoogleScholarGoogle Scholar |

Mcinnes RS, Carne PB (1978) Predation of cossid moth larvae by Yellow-tailed Black Cockatoos causing losses in plantations of Eucalyptus grandis in north coastal New South Wales. Wildlife Research 5, 101–121.
Predation of cossid moth larvae by Yellow-tailed Black Cockatoos causing losses in plantations of Eucalyptus grandis in north coastal New South Wales.Crossref | GoogleScholarGoogle Scholar |

McNab A, Sanders MG (2014) Consumption of exotic grass seeds (Poaceae: Cynodon dactylon) by the Eastern Ground Parrot (Pezoporous wallicus). Queensland Naturalist 52, 82–84. https://search.informit.org/doi/10.3316/informit.863219475618836

Mendes CP, Ribeiro MC, Galetti M (2016) Patch size, shape and edge distance influence seed predation on a palm species in the Atlantic forest. Ecography 39, 465–475.
Patch size, shape and edge distance influence seed predation on a palm species in the Atlantic forest.Crossref | GoogleScholarGoogle Scholar |

Miller AD, Nitschke C, Weeks AR, Weatherly WL, Heyes SD, Sinclair SJ, Holland OJ, Stevenson A, Broadhurst L, Hoebee SE, Sherman CDH, Morgan JW PMID: (2020) Genetic data and climate niche suitability models highlight the vulnerability of a functionally important plant species from south-eastern Australia. Evolutionary Applications 13, 2014–2029.
Genetic data and climate niche suitability models highlight the vulnerability of a functionally important plant species from south-eastern Australia.Crossref | GoogleScholarGoogle Scholar |

Moore G (2022) The impact of Yellow-tailed Black-Cockatoo ‘Calyptorhynchus funereus’ (Shaw, 1794) feeding on a Monterey Pine Pinus radiata D.Don. The Victorian Naturalist 139, 13–20. https://search.informit.org/doi/10.3316/informit.334288469779684

Morgan JW (1995) Ecological studies of the endangered Rutidosis leptorrhynchoides. I. Seed production, soil seed bank dynamics, population density and their effects on recruitment. Australian Journal of Botany 43, 1–11.
Ecological studies of the endangered Rutidosis leptorrhynchoides. I. Seed production, soil seed bank dynamics, population density and their effects on recruitment.Crossref | GoogleScholarGoogle Scholar |

Muff S, Nilsen EB, O’Hara RB, Nater CR PMID: (2022) Rewriting results sections in the language of evidence. Trends in Ecology & Evolution 37, 203–210.
Rewriting results sections in the language of evidence.Crossref | GoogleScholarGoogle Scholar |

Onofri A (2022) drcte: statistical approaches for time-to-event data in agriculture. R package version 1.0.6. Available at https://www.statforbiology.com

Onofri A, Benincasa P, Mesgaran MB, Ritz C (2018) Hydrothermal-time-to-event models for seed germination. European Journal of Agronomy 101, 129–139.
Hydrothermal-time-to-event models for seed germination.Crossref | GoogleScholarGoogle Scholar |

Onofri A, Piepho H-P, Kozak M (2019) Analysing censored data in agricultural research: a review with examples and software tips. Annals of Applied Biology 174, 3–13.
Analysing censored data in agricultural research: a review with examples and software tips.Crossref | GoogleScholarGoogle Scholar |

Pickup M, Young AG PMID: (2008) Population size, self-incompatibility and genetic rescue in diploid and tetraploid races of Rutidosis leptorrhynchoides (Asteraceae). Heredity 100, 268–274.
Population size, self-incompatibility and genetic rescue in diploid and tetraploid races of Rutidosis leptorrhynchoides (Asteraceae).Crossref | GoogleScholarGoogle Scholar |

Pizo MA, Vieira EM (2004) Granivorous birds as potentially important post-dispersal seed predators in a Brazilian forest fragment. Biotropica 36, 417–423.
Granivorous birds as potentially important post-dispersal seed predators in a Brazilian forest fragment.Crossref | GoogleScholarGoogle Scholar |

Possingham HP (1986) The Funereal Cockatoo on Eyre Peninsula. South Australian Ornithologist 30, 1–4.

R Core Team (2021) ‘R: a language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria). Available at https://www.R-project.org/

Salazar A, Goldstein G, Franco AC, Miralles-Wilhelm F (2012) Seed limitation of woody plants in Neotropical savannas. Plant Ecology 213, 273–287.
Seed limitation of woody plants in Neotropical savannas.Crossref | GoogleScholarGoogle Scholar |

Scott JK, Black R (1981) Selective predation by White-tailed Black Cockatoos on fruit of Banksia attenuata containing the seed-eating weevil Alphitopis nivea. Australian Wildlife Research 8, 421–430.
Selective predation by White-tailed Black Cockatoos on fruit of Banksia attenuata containing the seed-eating weevil Alphitopis nivea.Crossref | GoogleScholarGoogle Scholar |

Seburanga JL (2014) Evidence for pre-dispersal predation of seeds of Tithonia diversifolia by the black-faced canary (Serinus capistratus). Journal of Plant Interactions 9, 832–837.
Evidence for pre-dispersal predation of seeds of Tithonia diversifolia by the black-faced canary (Serinus capistratus).Crossref | GoogleScholarGoogle Scholar |

Severns P (2003) Inbreeding and small population size reduce seed set in a threatened and fragmented plant species, Lupinus sulphureus ssp. kincaidii (Fabaceae). Biological Conservation 110, 221–229.
Inbreeding and small population size reduce seed set in a threatened and fragmented plant species, Lupinus sulphureus ssp. kincaidii (Fabaceae).Crossref | GoogleScholarGoogle Scholar |

Sinclair SJ, Atchison K (2012) The pre-colonial distribution of grasslands, woodlands and forests on the Werribee plains, Victoria. Cunninghamia 12, 213–227.
The pre-colonial distribution of grasslands, woodlands and forests on the Werribee plains, Victoria.Crossref | GoogleScholarGoogle Scholar |

Stephens PA, Sutherland WJ, Freckleton RP (1999) What is the Allee effect? Oikos 87, 185–190.
What is the Allee effect?Crossref | GoogleScholarGoogle Scholar |

Stock WD, Finn H, Parker J, Dods K PMID: (2013) Pine as fast food: foraging ecology of an endangered cockatoo in a forestry landscape. PLoS ONE 8, e61145
Pine as fast food: foraging ecology of an endangered cockatoo in a forestry landscape.Crossref | GoogleScholarGoogle Scholar |

Taylor A (1988) ‘The Banksia Atlas.’ (Australian Government Publishing Service: Canberra, ACT, Australia)

Tella JL, Blanco G, Dénes FV, Hiraldo F (2019) Overlooked parrot seed dispersal in Australia and South America: insights on the evolution of dispersal syndromes and seed size in Araucaria trees. Frontiers in Ecology and Evolution 7, 82
Overlooked parrot seed dispersal in Australia and South America: insights on the evolution of dispersal syndromes and seed size in Araucaria trees.Crossref | GoogleScholarGoogle Scholar |

Tschumi M, Ekroos J, Hjort C, Smith HG, Birkhofer K PMID: (2018) Rodents, not birds, dominate predation-related ecosystem services and disservices in vertebrate communities of agricultural landscapes. Oecologia 188, 863–873.
Rodents, not birds, dominate predation-related ecosystem services and disservices in vertebrate communities of agricultural landscapes.Crossref | GoogleScholarGoogle Scholar |

Vaughton G (1990) Predation by insects limits seed production in Banksia spinulosa var. neoanglica (Proteaceae). Australian Journal of Botany 38, 335–340.
Predation by insects limits seed production in Banksia spinulosa var. neoanglica (Proteaceae).Crossref | GoogleScholarGoogle Scholar |

Vaz Ferreira A, Bruna EM, Vasconcelos HL (2011) Seed predators limit plant recruitment in Neotropical savannas. Oikos 120, 1013–1022.
Seed predators limit plant recruitment in Neotropical savannas.Crossref | GoogleScholarGoogle Scholar |

Veldman JW, Greg Murray K, Hull AL, Mauricio Garcia-C J, Mungall WS, Rotman GB, Plosz MP, Mcnamara LK (2007) Chemical defense and the persistence of pioneer plant seeds in the soil of a tropical cloud forest. Biotropica 39, 87–93.
Chemical defense and the persistence of pioneer plant seeds in the soil of a tropical cloud forest.Crossref | GoogleScholarGoogle Scholar |

Villaseñor-Sánchez EI, Dirzo R, Renton K (2010) Importance of the lilac-crowned parrot in pre-dispersal seed predation of Astronium graveolens in a Mexican tropical dry forest. Journal of Tropical Ecology 26, 227–236.
Importance of the lilac-crowned parrot in pre-dispersal seed predation of Astronium graveolens in a Mexican tropical dry forest.Crossref | GoogleScholarGoogle Scholar |

Warr SJ, Thompson K, Kent M PMID: (1992) Antifungal activity in seed coat extracts of woodland plants. Oecologia 92, 296–298.
Antifungal activity in seed coat extracts of woodland plants.Crossref | GoogleScholarGoogle Scholar |

Way SL, van Weenen J (2008) Eyre Peninsula yellow-tailed Black Cockatoo (Calyptorhynchus funereus whitei) Regional Recovery Plan. Department for Environment and Heritage, South Australia.

Wickham H (2016) ‘ggplot2: elegant graphics for data analysis.’ (Springer-Verlag: New York, NY, USA). Available at https://ggplot2.tidyverse.org

Witkowski ETF, Lamont BB, Connell SJ (1991) Seed bank dynamics of three co-occurring Banksias in south coastal Western Australia: the role of plant age, cockatoos, senescence and interfire establishment. Australian Journal of Botany 39, 385–397.
Seed bank dynamics of three co-occurring Banksias in south coastal Western Australia: the role of plant age, cockatoos, senescence and interfire establishment.Crossref | GoogleScholarGoogle Scholar |

Wright BR, Zuur AF, Chan GCK (2014) Proximate causes and possible adaptive functions of mast seeding and barren flower shows in spinifex grasses (Triodia spp.) in arid regions of Australia. The Rangeland Journal 36, 297–308.
Proximate causes and possible adaptive functions of mast seeding and barren flower shows in spinifex grasses (Triodia spp.) in arid regions of Australia.Crossref | GoogleScholarGoogle Scholar |

Xia J, Sun S, Liu G PMID: (2013) Evidence of a component Allee effect driven by predispersal seed predation in a plant (Pedicularis rex, Orobanchaceae). Biology Letters 9, 20130387
Evidence of a component Allee effect driven by predispersal seed predation in a plant (Pedicularis rex, Orobanchaceae).Crossref | GoogleScholarGoogle Scholar |

Yates CJ, Hobbs RJ (1997) Temperate Eucalypt woodlands: a review of their status, processes threatening their persistence and techniques for restoration. Australian Journal of Botany 45, 949–973.
Temperate Eucalypt woodlands: a review of their status, processes threatening their persistence and techniques for restoration.Crossref | GoogleScholarGoogle Scholar |

Young A, Miller C, Gregory E, Langston A (2000) Sporophytic self-incompatibility in diploid and tetraploid races of Rutidosis leptorrhynchoides (Asteraceae). Australian Journal of Botany 48, 667–672.
Sporophytic self-incompatibility in diploid and tetraploid races of Rutidosis leptorrhynchoides (Asteraceae).Crossref | GoogleScholarGoogle Scholar |